象耳豆根结线虫分泌的分支酸变位酶效应蛋白操控寄主免疫以促进寄生

doi:10.1016/j.jia.2023.11.039

Journal of Integrative Agriculture ›› 2024, Vol. 23 ›› Issue (12): 4107-4119.DOI: 10.1016/j.jia.2023.11.039

象耳豆根结线虫分泌的分支酸变位酶效应蛋白操控寄主免疫以促进寄生

收稿日期:2023-04-29 接受日期:2023-10-07 出版日期:2024-12-20 发布日期:2024-11-15

A novel chorismate mutase effector secreted from root-knot nematode Meloidogyne enterolobii manipulates plant immunity to promote parasitism

Tuizi Feng^{1, 2*}, Yuan Chen^{1, 2*}, Zhourong Li¹, Ji Pei¹, Deliang Peng³, Huan Peng^3#, Haibo Long^{1, 2#}

¹Key Laboratory of Integrated Pest Management on Tropical Crops, Ministry of Agriculture and Rural Affairs, Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China
²Hainan Key Laboratory for Monitoring and Control of Tropical Agricultural Pests, Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China
³State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China

Received:2023-04-29 Accepted:2023-10-07 Online:2024-12-20 Published:2024-11-15
About author:Tuizi Feng, E-mail: fengtuizi@catas.cn; Yuan Chen, E-mail: chenyuan@catas.cn; #Correspondence Haibo Long, Tel: +86-898-66969231, E-mail: longhb@catas.cn; Huan Peng, E-mail: penghuan@caas.cn * These authors contributed equally to this study.
Supported by:
This work was supported by the Hainan Provincial Natural Science Foundation of China (323MS102 and 320QN307) and Central Public-Interest Scientific Institution Basal Research Fund, China (1630042022008).

摘要/Abstract

摘要：

根结线虫（Meloidogyne spp.）是一种在全球范围内广泛分布的、具有重要经济意义的植物寄生线虫。为了成功寄生并对抗寄主免疫系统，植物寄生线虫会分泌效应蛋白以促进侵染。本研究中，我们从象耳豆根结线虫（M. enterolobii）中鉴定了一种分支酸变位酶效应蛋白，命名为Me-CM。原位杂交实验结果表明Me-cm基因在食道腺中特异表达，且在根结线虫寄生阶段转录水平上调表达。体内以及体外RNA沉默实验结果证明，Me-CM影响了象耳豆根结线虫的致病性，降低了寄主感染率、根结数量、卵囊数、每个卵囊内的卵粒数和繁殖系数。亚细胞定位结果表明Me-CM蛋白定位在植物细胞的细胞质和细胞核中。通过检测拟南芥野生型和Me-cm过表达株系寄主免疫相关基因的转录水平，发现Me-cm基因过表达干扰了相关基因正常转录，尤其是降低了水杨酸合成途径标记基因PR1的转录水平。进一步检测拟南芥过表达株系的水杨酸含量表明，Me-cm基因的过表达可显著降低寄主水杨酸浓度，进而影响寄主免疫防御反应。本研究表明，象耳豆根结线虫可能通过分泌分支酸变位酶效应蛋白Me-CM干扰寄主水杨酸信号通路，影响寄主免疫反应，最终促进根结线虫的寄生。综上所述，本研究揭示了象耳豆根结线虫分泌的分支酸变位酶效应蛋白Me-CM调控寄主对象耳豆根结线虫感病性的作用机制，可作为利用RNAi技术开发抗性品种的潜在分子靶标。

Abstract:

Meloidogyne spp. is an economically important plant-parasitic nematode distributed worldwide. To fight with host immune system for successful parasitism, plant parasitic nematodes secrete effectors to promote infection. In this study, we identified one chorismate mutase (CM) effector from M. enterolobii, named Me-CM. Spatial and temporal expression assays exhibited Me-cm is expressed in esophageal glands and up-regulated at parasitic-stage juveniles. Me-CM affects the pathogenicity of M. enterolobii based on the reduced infection rate, number of galls, egg masses, eggs per mass and multiplication rate collected from RNA silencing experiments. We showed that Me-CM localized in the cytoplasm and nucleus of plant cells and decreased the expression level of the marker gene PR1 of salicylic acid (SA) pathway. Besides, constitutive expression of Me-cm in Arabidopsis thaliana significantly reduced salicylic acid concentration. These results suggested that M. enterolobii may secrete effector Me-CM to fight with plant immune systems via regulating SA signaling pathway when interacting with host plants, ultimately facilitating parasitism.

Key words: Meloidogyne enterolobii , effector , chorismate mutase , salicylic acid , plant immunity

Tuizi Feng, Yuan Chen, Zhourong Li, Ji Pei, Deliang Peng, Huan Peng, Haibo Long. 象耳豆根结线虫分泌的分支酸变位酶效应蛋白操控寄主免疫以促进寄生[J]. Journal of Integrative Agriculture, 2024, 23(12): 4107-4119.

Tuizi Feng, Yuan Chen, Zhourong Li, Ji Pei, Deliang Peng, Huan Peng, Haibo Long. A novel chorismate mutase effector secreted from root-knot nematode Meloidogyne enterolobii manipulates plant immunity to promote parasitism[J]. Journal of Integrative Agriculture, 2024, 23(12): 4107-4119.

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象耳豆根结线虫分泌的分支酸变位酶效应蛋白操控寄主免疫以促进寄生

A novel chorismate mutase effector secreted from root-knot nematode Meloidogyne enterolobii manipulates plant immunity to promote parasitism

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